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325 original Evolution, Medicine, and Public Health [2016] pp. 325–337 research doi:10.1093/emph/eow027 article The blemishes of modern society? Acne prevalence in the Dogon of Mali Christine E. Campbell1 and Beverly I. Strassmann*,1 1Department of Anthropology & Institute for Social Research, University of Michigan, Ann Arbor, MI, USA *Corresponding author. Department of Anthropology & Research Center for Group Dynamics, University of Michigan, 426 Thompson St, Ann Arbor, MI 48104, USA. E-mail: [email protected] Received 26 May 2016; revised version accepted 00 0000 ABSTRACT Background and Objectives: Non-communicable diseases may reflect an evolutionary mismatch be- tween our human ancestry and modern environments. To explore the mismatch hypothesis for Acne vulgaris, we studied the prevalence and severity of acne in Dogon adolescents in Mali, West Africa. Methodology: We graded the prevalence and severity of acne in 1182 Dogon adolescents aged 11–18 years from nine villages using facial photos taken as part of a prospective cohort study. Eighty-nine (89%) of the individuals in the cohort migrated to the city during adolescence, enabling us to assess the effect of urban migration. Using multivariable logistic regression, we estimated the effect of predictor variables on the presence of acne. Results: The prevalence of acne in the cohort was 28%, with 90% of cases being mild or very mild. Thus, the prevalence and severity of acne was much lower than for adolescents in high-income countries. Controlling for age, puberty, and body mass index (BMI), the odds of boys developing acne was 85% lower in the city than in the villages (P = 0.002). Conclusion and Implications: Acne is similar to the ‘diseases of civilization’ in being promoted by the pro-inflammatory properties of modern diets. The low prevalence and severity of acne in the Dogon supports the mismatch hypothesis and suggests that acne should join the list of diseases of modern lifestyles. However, we also observed an unexpected decrease in acne in urban boys. Future research is needed for a deeper mechanistic understanding of the interplay between diet, inflammation, immune function and other environmental exposures that differ between urban and rural environments. INTRODUCTION significant perception of disfigurement [3,7], In high-income countries, Acne vulgaris is one of the decreased self-esteem [7], depression [8] and lower most common skin diseases [1–5] and one of the prospects for employment [9]. Acne vulgaris is a most frequent diagnoses for patients who visit a multifactorial disease [10,11] that is influenced by dermatologist [6]. Although not life threatening, four agreed upon factors: (1) hyperkeratinization the lesions and scarring of Acne vulgaris can cause and obstruction of sebaceous follicles caused by ß The Author(s) 2016. Published by Oxford University Press on behalf of the Foundation for Evolution, Medicine, and Public Health. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 326 | Campbell and Strassmann Evolution, Medicine, and Public Health abnormal desquamation of the follicular epithelium; Here we report the prevalence and severity of acne (2) androgen-stimulated increase in sebum produc- in Dogon adolescents in Mali, West Africa. We tion, (3) colonization of hair follicles in the skin by hypothesized a low prevalence and severity of acne Propionibacterium acnes, and (4) inflammation in the Dogon on account of their traditional life-style, [4,5,12–14]. The pathogenesis of acne is similar including a diet based on millet farming with across different ethnic populations [6] and acne limited consumption of novel, pro-inflammatory, has been documented within all Fitzpatrick skin fast foods. Inflammation plays an important role in types (The Fitzpatrick scale is a numerical classifica- the development of acne [27] and in the aetiology of tion of skin color from I to VI with Type I being the other chronic diseases [28] associated with modern fairest (albino, very fair with freckles) to Type VI lifestyles. Examples include cardiovascular disease being the darkest (deeply pigmented, 0black0 skin)) [29,30] type 2 diabetes mellitus [29], Alzheimer’s dis- [6,15]. Here we consider Acne vulgaris within the ease [31], and various cancers [32]. Modern dietary framework of evolutionary medicine. habits promote inflammation, especially consump- Human bodies are imperfectly adapted for a var- tion of foods that have a high glycemic load or a high iety of reasons including the ‘mismatch’ between ratio of omega-6 to omega-3 polyunsaturated fatty our genes and novel features of the environment acids (PUFAs) [28]. The evidence that pro-inflamma- [16]. However, there was no singular Environment tory foods simultaneously exacerbate acne [4] and of Evolutionary Adaptedness or specific time-period other chronic diseases [28], raises the possibility that of our evolutionary past to which humans are Acne vulgaris (especially inflammatory acne) should adapted [17–19]. Instead different aspects of human be added to the list of ‘diseases of civilization’. biology evolved in different time periods [19,20]. The We also hypothesized that acne in the Dogon is aggravated by urban migration—a globally import- early emphasis on Stone Age genes was unwar- ant source of environmental novelty in the 21st cen- ranted [21] as many genes are far older (e.g. Hox tury. The world’s population is >50% urban and will genes) and others are more recent than the be 66% urban by 2050 [33]. The Dogon are migrating Pleistocene (e.g. genes for lactase persistence) to Bamako, which is the fastest growing city in Africa [20,22]. Nor was the advent of agriculture the only and the sixth fastest growing city in the world [34]. disease-inducing transition in the human past [19]. When rural adolescents from farming families move Environmental and lifestyle changes relevant to dis- to the city, they are introduced to a radically different ease risk occurred both long before and long after environment compared to the one they experienced the end of the Stone Age [19]. during development. In the city, one might expect a Although it is helpful to put the Stone Age in per- more acnegenic diet due to increased consumption spective, discarding the mismatch hypothesis is un- of pro-inflammatory foods such as red meat [35] milk justifiable. When the environment changes, traits [36], food with a high glycemic index [12, 37–40], or a that were adaptive in the previous environment be- high ratio of omega-6 to omega-3 fatty acids [42–46]. come maladaptive in the new environment until nat- One might also expect increased psychosocial stress ural selection has ‘caught up’. Quite simply, natural due to loss of kin support or increased competition selection takes time to act [23–25]. A striking ex- from wealthy urbanites. Further, in the city people ample was proposed by Janzen and Martin (1982) tend to be more sedentary and do not get the stress- [26], who studied the peculiarly large and hard fruits reducing benefits of aerobic farm work [47]. of many trees in the tropical forests of Central Previous studies reported a low prevalence of America. These fruits appear to be anachronistically acne in traditional populations. For example, the adapted for dispersal by gomphotheres (a relative of prevalence of acne was 0% in the Kitavan Islanders the mastodon with powerful molar teeth) and other of Papua New Guinea and the Ache´ foragers of large mammals that went extinct about 10 000 years Paraguay [4], 6.9% in adolescents of a roadside ago. Ten millennia has not been long enough for the Ethiopian community [48], and 4.2% in adolescents evolution of fruits that will be eaten and dispersed by in a cross-sectional, hospital-based study in Mali smaller mammals, so these overly-large and overly- [49]. Furthermore, several studies reported that the protected fruits rot under their parent trees [24,26]. Inuit [50] and Chinese [51] only developed acne after Similarly, our study of acne is predicated on the transitioning to a modern lifestyle. However, these understanding that after the environment changes, studies [4, 48] had very small sample sizes of ado- it will take time for natural selection to catch up. lescents: from 47 to 300 individuals (Table 1). Our The blemishes of modern society? Table 1. Studies of adolescent acne prevalence by country Background of Community Studied Country Age (years) N Total Moderate to Referenceb Prevalence (%) Severe (% of Total Prevalence) Subsistence horticulture, fisherman Papua New Guinea 15–25 300 00 Cordain et al. 2002 Roadside town of 4000, subsistence farming Ethiopia 10–16 47 2.7 NRa Figueroa et al. 1996 Millet farming, rural villages, Mali 11–18 1182 28.4 9.2 This study & city of 2 million 10 rural villages of Kakamega county Kenya 10–19 133 38.3 N/A Kiprono et al. 2015 Students in town of Arequipa, Peru 12–18 2214 41.7 19.0 Freye et al.1998 population 800,000 Secondary school in Nottingham, United Kingdom 14–16 317 50.0 27.4 Smithard et al. 2001 population 310,000 Eskisehir province (developed) and Turkey 13–18 2230 60.0 21.4 Aksu et al. 2011 surroundings (rural) Randomly selected secondary schools New Zealand 12–18 9398 67.3 20.9 Purvis et al. 2004 Secondary schools in state of Victoria Australia 13–18 797 83.5 21.0 Kilkenny et al. 1998 Secondary schools and colleges Singapore 13–19 1045 88.0 48.6 Tan et al. 2007 Schools in Kaduna, population 1.5 million Nigeria 11–19 418 90.7 7.3 Yahya 2009 Students in Tehran, population 8 million Iran 12–20 1,002 93.2 15.0 Ghodsi et al.

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